Journal of Neurophysiology, Vol 76, Issue 6 3834-3841, Copyright © 1996 by APS

ARTICLES

Activation of pharmacologically distinct metabotropic glutamate receptors depresses reticulospinal-evoked monosynaptic EPSPs in the lamprey spinal cord

P. Krieger, A. el Manira and S. Grillner
Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.

1. Different metabotropic glutamate receptors (mGluRs) can modulate synaptic transmission in different regions in the CNS, but their roles at individual synaptic connections have not been detailed. We used paired intracellular recordings from reticulospinal axons and their postsynaptic target neurons in the lamprey spinal cord to investigate the effects of mGluR activation on glutamatergic synaptic transmission. 2. The mGluR agonists (1S,3R)-1-aminocyclopentane-1,3-dicarboxyylic acid [(1S,3R)-ACPD] and L(+)-2-amino-4-phosphonobutyric acid (L-AP4) both reduced the amplitude of monosynaptic excitatory postsynaptic potentials (EPSPs) elicited by stimulation of single reticulospinal axons. The depression of monosynaptic unitary EPSPs occurred without any apparent change in the input resistance of postsynaptic neurons. Furthermore, the mGluR agonists did not affect the amplitude of (RS)-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-induced depolarizations. Taken together, these results thus suggest that (1S,3R)-ACPD and L-AP4 depress reticulospinal synaptic transmission via presynaptic mechanisms. 3. (2S,1'S,2'S)-2-(carboxycyclopropyl) glycine (L-CCG-I), which selectively activates group II mGluRs, also reduced the amplitude of reticulospinal-evoked EPSPs without any apparent change in the input resistance or membrane potential of the postsynaptic neuron. 4. The mGluR antagonist alpha-methyl-L-AP4 blocked the depression induced by L-AP4 but not that induced by (1S,3R)-ACPD. Furthermore, the effects of coapplication of (1S,3R)-ACPD and L-AP4 were additive, suggesting that they inhibit synaptic transmission by an action on pharmacologically distinct mGluRs. 5. These results provide evidence for the colocalization of at least two different subtypes of presynaptic mGluRs on a single reticulospinal axon in the lamprey. These presynaptic mGluRs could serve as glutamatergic autoreceptors limiting the extent of reticulospinal-mediated excitation of spinal neurons.

This article has been cited by other articles:

				E. Nanou, A. Kyriakatos, P. Kettunen, and A. El Manira Separate signalling mechanisms underlie mGluR1 modulation of leak channels and NMDA receptors in the network underlying locomotion J. Physiol., June 15, 2009; 587(12): 3001 - 3008. [Abstract] [Full Text] [PDF]

				K. A. Quinlan and J. T. Buchanan Cellular and Synaptic Actions of Acetylcholine in the Lamprey Spinal Cord J Neurophysiol, August 1, 2008; 100(2): 1020 - 1031. [Abstract] [Full Text] [PDF]

				P. Wallen, B. Robertson, L. Cangiano, P. Low, A. Bhattacharjee, L. K. Kaczmarek, and S. Grillner Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons J. Physiol., November 15, 2007; 585(1): 75 - 90. [Abstract] [Full Text] [PDF]

				A. Jackson, S. N. Baker, and E. E. Fetz Tests for presynaptic modulation of corticospinal terminals from peripheral afferents and pyramidal tract in the macaque J. Physiol., May 15, 2006; 573(1): 107 - 120. [Abstract] [Full Text] [PDF]

				P. Kettunen, D. Hess, and A. E. Manira mGluR1, But Not mGluR5, Mediates Depolarization of Spinal Cord Neurons by Blocking a Leak Current J Neurophysiol, October 1, 2003; 90(4): 2341 - 2348. [Abstract] [Full Text] [PDF]

				S. Alford, E. Schwartz, and G. V. Di Prisco The Pharmacology of Vertebrate Spinal Central Pattern Generators Neuroscientist, June 1, 2003; 9(3): 217 - 228. [Abstract] [PDF]

				P. Kettunen, P. Krieger, D. Hess, and A. El Manira Signaling Mechanisms of Metabotropic Glutamate Receptor 5 Subtype and Its Endogenous Role in a Locomotor Network J. Neurosci., March 1, 2002; 22(5): 1868 - 1873. [Abstract] [Full Text] [PDF]

				H Daniel and F Crepel Control of Ca2+ influx by cannabinoid and metabotropic glutamate receptors in rat cerebellar cortex requires K+ channels J. Physiol., December 15, 2001; 537(3): 793 - 800. [Abstract] [Full Text] [PDF]

				S. Grillner, P. Wallen, R. Hill, L. Cangiano, and A. E. Manira Ion channels of importance for the locomotor pattern generation in the lamprey brainstem-spinal cord J. Physiol., May 15, 2001; 533(1): 23 - 30. [Abstract] [Full Text] [PDF]

				F. Aoki, T. Wannier, and S. Grillner Slow Dorsal-Ventral Rhythm Generator in the Lamprey Spinal Cord J Neurophysiol, January 1, 2001; 85(1): 211 - 218. [Abstract] [Full Text] [PDF]

				A. El Manira and P. Wallen Mechanisms of Modulation of a Neural Network Physiology, August 1, 2000; 15(4): 186 - 191. [Abstract] [Full Text] [PDF]

				P. Krieger, J. Hellgren-Kotaleski, P. Kettunen, and A. J. El Manira Interaction between Metabotropic and Ionotropic Glutamate Receptors Regulates Neuronal Network Activity J. Neurosci., July 15, 2000; 20(14): 5382 - 5391. [Abstract] [Full Text] [PDF]

				N. E. Schwartz and S. Alford Physiological Activation of Presynaptic Metabotropic Glutamate Receptors Increases Intracellular Calcium and Glutamate Release J Neurophysiol, July 1, 2000; 84(1): 415 - 427. [Abstract] [Full Text] [PDF]

				D. Parker Presynaptic and Interactive Peptidergic Modulation of Reticulospinal Synaptic Inputs in the Lamprey J Neurophysiol, May 1, 2000; 83(5): 2497 - 2507. [Abstract] [Full Text] [PDF]

				D. Parker Activity and Calcium-Dependent Mechanisms Maintain Reliable Interneuron Synaptic Transmission in a Rhythmic Neural Network J. Neurosci., March 1, 2000; 20(5): 1754 - 1766. [Abstract] [Full Text] [PDF]

				P. Krieger, A. Buschges, and A. el Manira Calcium Channels Involved in Synaptic Transmission From Reticulospinal Axons in Lamprey J Neurophysiol, April 1, 1999; 81(4): 1699 - 1705. [Abstract] [Full Text] [PDF]

				H. von Gersdorff, R. Schneggenburger, S. Weis, and E. Neher Presynaptic Depression at a Calyx Synapse: The Small Contribution of Metabotropic Glutamate Receptors J. Neurosci., November 1, 1997; 17(21): 8137 - 8146. [Abstract] [Full Text] [PDF]